Skip to main content
SpringerLink
Log in

Exposure to 17α-ethynylestradiol causes dose and temporally dependent changes in intersex, females and vitellogenin production in the Sydney rock oyster

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Although mounting evidence suggests exposure to estrogenic contaminants increases vitellogenin production in molluscs, demonstration of dose–response relationships and knowledge of the temporal nature of the vitellogenin response with continual exposure is currently lacking for biomarker utility. To address this knowledge gap, adult Sydney rock oysters, Saccostrea glomerata, were exposed to a range of environmentally relevant concentrations of 17α-ethynylestradiol (EE2) (0, 6.25, 12.5, 25 or 50 ng/l) in seawater under laboratory conditions. Vitellogenin induction and gonadal development was assessed following 4, 21 and 49 days exposure to EE2. Vitellogenin was found to increase in a dose dependent manner with EE2 exposure for females (4 and 49 days) and males (4 and 21 days). Histological examination of gonads revealed a number of individuals exhibited intersex (ovotestis) in 50 ng/l EE2 (after 21 days) and in 6.25 and 12.5 ng/l EE2 (after 49 days). Furthermore, a significant shift towards females was observed following 49 days exposure at 50 ng/l EE2 suggesting estrogenic exposure is capable of facilitating a progression for protandric males from male-intersex-female gametal status. Increases in female vitellogenin (4 days) were predictive of later increases in female developmental stages at 21 days and increases in oocyte area following 49 days. Male vitellogenin (4 days) was predictive of decreased male percentages and lower male developmental stages at 49 days. Vitellogenin in S. glomerata is a predictive biomarker of estrogenic exposure and effect if sampled soon after exposure and at the commencement of a gonadal development cycle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aherne G, Briggs R (1989) The relevance of the presence of certain synthetic steroids in the aquatic environment. J Pharm Pharmacol 41:735–736

    CAS  Google Scholar 

  • Andersen H, Siegrist H, Halling-Sørensen B, Ternes T (2003) Fate of estrogens in a municipal sewage treatment plant. Environ Sci Technol 37:4021–4026

    Article  CAS  Google Scholar 

  • Andrew M, Dunstan RH, O’Connor WA, Van Zwieten L, Nixon B, MacFarlane GR (2008) Effects of 4-nonylphenol and 17α-ethynylestradiol exposure in the Sydney rock oyster, Saccostrea glomerata: vitellogenin induction and gonadal development. Aquat Toxicol 88:39–47

    Article  CAS  Google Scholar 

  • Asif M (1979) Hermphroditism and sex reversal in the four common oviparous species of oysters from the coast of Karachi. Hydrobiologia 66(1):49–55

    Article  Google Scholar 

  • A.S.T.M. (1996) Standard guide for conducting acute toxicity tests with fishes, macro invertebrates, and amphibians. E729-96. In: Annual book of ASTM Standards, vol 11.05. Philadelphia, PA

  • Belfroid A, Van der Horst A, Vethaak A, Schäfer A, Rijs G, Wegener J, Confino W (1999) Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in The Netherlands. Sci Total Environ 225:101–108

    Article  CAS  Google Scholar 

  • Beninger PG, Le Pennec M (2003) Structure and function in scallops. In: Shumway SE, Parsons G (eds) Scallops: biology, ecology and aquaculture, 2nd edn. Elsevier, Amsterdam, pp 133–191

    Google Scholar 

  • Blaise C, Gagné F, Pellerin J, Hansen P (1999) Determination of vitellogenin-like properties in Mya arenaria hemolymph (Saguenay Fjord, Canada): a potential bio-marker for endocrine disruption. Environ Toxicol Chem 4:455–465

    Google Scholar 

  • Blaise C, Gagné F, Salazar M, Salazar S, Trottier S, Hansen P (2003) Experimentally-induced feminisation of freshwater mussels after long-term exposure to a municipal effluent. Fresenius Environ Bull 12(8):865–870

    CAS  Google Scholar 

  • Cox E, Smith M, Nell A, Maguire G (1996) Studies on triploid oysters in Australia. VI. Gonadal development in diploid and triploid Sydney rock oysters Saccostrea commercialis (Iredale and Roughley). J Exp Mar Biol Ecol 197:101–120

    Article  Google Scholar 

  • Desbrow C, Routledge E, Brightly G, Sumpter J, Waldock M (1998) Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environ Sci Technol 32(11):1549–1558

    Article  CAS  Google Scholar 

  • Dinamani P (1974) Reproductive cycle and gonadial changes in the New Zealand rock oyster Crassostrea glomerata. N Z J Mar Freshw Res 8(1):39–65

    Article  Google Scholar 

  • Gagné F, Blaise C (2000) Organic alkali-labile phosphates in biological materials: a generic assay to detect vitellogenin in biological tissues. Environ Toxicol 15:243–247

    Article  Google Scholar 

  • Gagné F, Blaise C, Salazar M, Salazar S, Hansen P (2001) Evaluation of estrogenic effects of municipal effluents to the freshwater mussel Elliptio complanata. Comp Biochem Physiol C 128:213–225

    Article  Google Scholar 

  • Gagné F, Blaise C, Pellerin J, Gauthier-Clerc S (2002) Alteration of the biochemical properties of female gonads and vitellins in the clam Mya arenaria at contaminated sites in the Saguenay Fjord. Mar Environ Res 53:295–310

    Article  Google Scholar 

  • Gagné F, André C, Blaise C (2005) Increased vitellogenin gene expression in the mussel Elliptio complanata exposed to estradiol-17β. Fresenius Environ Bull 14(10):861–866

    Google Scholar 

  • Gagné F, Blaise C, Pellerin J, Pellerin E, Strand J (2006) Health status of Mya arenaria bivalves collected from contaminated sites in Canada (Saguenay Fjord) and Denmark (Odense Fjord) during their reproductive period. Ecotoxicol Environ Saf 64:348–361

    Article  Google Scholar 

  • Gagnon C, Gagné F, Turcotte P, Saulnier I, Blaise C, Salazar M, Salazar S (2006) Exposure of caged mussels to metals in a primary-treated municipal wastewater plume. Chemosphere 62:998–1010

    Article  CAS  Google Scholar 

  • Guo X, Hedgecock D, Hershberger W, Cooper K, Allen S (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas. Evolution 52(2):394–399

    Article  Google Scholar 

  • Howard D, Smith C (1983) Histological techniques for marine bivalve mollusks. NOAA Technical Memorandum NMFS-F/NEC-25. NOAA Scientific and Technical Publications, Woods Hole, MA, p 97

  • Huggett R, Kimerle R, Mehrle PJ, Bergman H (1989) BIOMARKERS: biochemical physiological and histological markers of anthropogenic stress. Lewis Publishers, Boca Raton, pp 235–335

    Google Scholar 

  • Kajiwara M, Kuraku S, Kurokawa T, Kato K, Toda S, Hirose H, Takahashi S, Shibata Y, Iguchi T, Matsumoto T, Miyata T, Miura T, Takahashi Y (2006) Tissue preferential expression of estrogen receptor gene in the marine snail, Thais clavigera. Gen Comp Endocrinol 148(3):315–326

    Article  CAS  Google Scholar 

  • Keay J, Bridgham J, Thornton J (2006) The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 147(8):3861–3869

    Article  CAS  Google Scholar 

  • Ketata I, Denier X, Hamza-Chaffai A, Minier C (2008) Endocrine related reproductive effects in molluscs. Comp Biochem Physiol C 147:261–270

    Google Scholar 

  • Lafont R, Mathieu M (2007) Steroids in aquatic invertebrates. Ecotoxicology 16:109–130

    Article  CAS  Google Scholar 

  • Langston W, Burt G, Chesman B, Vane C (2005) Partitioning, bioavailability and effects of oestrogens and xeno-oestrogens in the aquatic environment. J Mar Biol Assess UK 85:1–31

    Article  CAS  Google Scholar 

  • Langston W, Burt G, Chesman B (2007) Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Mar Ecol Prog Ser 333:173–184

    Article  CAS  Google Scholar 

  • Leaños-Castañeda O, Van Der Kraak G (2007) Functional characterization of estrogen receptor subtypes, ERα and ERβ, mediating vitellogenin production in the liver of rainbow trout. Toxic Appl Pharmacol 224(2):116–125

    Article  Google Scholar 

  • Li Q, Osada M, Suzuki T, Mori K (1998) Changes in vitellin during oogenesis and effect of estradiol-17b in the Pacific oyster, Crassostrea gigas. Invertebr Reprod Dev 33(1):87–93

    Google Scholar 

  • Lucas A, Beninger P (1985) The use of physiological condition indices in marine bivalve aquaculture. Aquaculture 44(3):187–200

    Article  Google Scholar 

  • Matozzo V, Marin M (2005) Can 4-nonylphenol induce vitellogenin-like proteins in the clam Tapes philippinarum? Environ Res 97(1):43–49

    Article  CAS  Google Scholar 

  • Matozzo V, Marin M (2008) Can 17β-estradiol induce vitellogenin-like proteins in the clam Tapes philippinarum? Environ Toxicol Pharmacol 26:38–44

    Article  CAS  Google Scholar 

  • Matozzo V, Gagné F, Marin M, Ricciardi F, Blaise C (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34:531–545

    Article  CAS  Google Scholar 

  • Matsumoto T, Osada M, Osawa Y, Mori K (1997) Gonadal estrogen profile and immunohistochemical localization of steroidogenic enzymes in the oyster and scallop during sexual maturation. Comp Biochem Physiol B 118(4):811–817

    Article  Google Scholar 

  • Matsumoto T, Nakamura A, Mori K, Kayano T (2003) Molecular characterisation of a cDNA encoding putative vitellogenin from the Pacific oyster Crassostrea gigas. Zool Sci 20:37–42

    Article  CAS  Google Scholar 

  • Matsumoto T, Nakamura A, Mori K, Akiyama T, Hirose H, Takahashi Y (2007) Oyster estrogen receptor: cDNA cloning and immunolocalization. Gen Comp Endocrinol 151(2):195–201

    Article  CAS  Google Scholar 

  • Mori K, Muramatsu T, Nakamura Y (1969) Effect of steroid on oyster. III. Sex reversal from male to female in Crassostrea gigas by estradiol-17B. Bull Jpn Soc Sci Fish 35(11):1072–1076

    CAS  Google Scholar 

  • Nice H, Morritt D, Crane M, Thorndyke M (2003) Long-term and transgenerational effects of nonylphenol exposure at a key stage in the development of Crassostrea gigas. Possible endocrine disruption? Mar Ecol Prog Ser 256:293–300

    Article  CAS  Google Scholar 

  • Ortiz-Zarragoitia M, Cajaraville M (2006) Biomarkers of exposure and reproduction-related effects in mussels exposed to endocrine disruptors. Arch Environ Contam Toxicol 50:361–369

    Article  CAS  Google Scholar 

  • Osada M, Takamura T, Sato H, Mori K (2003) Vitellogenin synthesis in the ovary of scallop, Patinopecten yessoensis: control by estradiol-17β and the central nervous system. J Exp Zool 299A:172–179

    Article  CAS  Google Scholar 

  • Pampanin D, Marangon I, Volpato E, Campesan G, Nasci C (2005) Stress biomarkers and alkali-labile phosphate level in mussels (Mytilus galloprovincialis) collected in the urban area of Venice (Venice Lagoon, Italy). Environ Pollut 136(1):103–107

    Article  CAS  Google Scholar 

  • Pipe R (1987) Ultrastructural and cytochemical study on interactions between nutrient storage cells and gametogenesis in the mussel Mytilus edulis. Mar Biol 96(4):519–528

    Article  Google Scholar 

  • Puinean AM, Labadie P, Hill EM, Osada M, Kishida M, Nakao R, Novillo A, Callard IP, Rotchell JM (2006) Laboratory exposure to 17α-estradiol fails to induce vitellogenin and estrogen receptor gene expression in the marine invertebrate Mytilus edulis. Aquat Toxicol 79:376–383

    Article  CAS  Google Scholar 

  • Ricciardi F, Matozzo V, Marin M (2008) Effects of 4-nonylphenol exposure in mussels (Mytilus galloprovincialis) and crabs (Carcinus aestuarii) with particular emphasis on vitellogenin induction. Mar Pollut Bull 57:365–372

    Article  CAS  Google Scholar 

  • Roughley TC (1933) The life history of the Australian oyster (Ostrea commercialis). Proc Linn Soc N S W 58:279–333

    Google Scholar 

  • Scanes P (1997) Oyster watch: monitoring trace metal and organochlorine concentrations in Sydney’s coastal waters. Mar Pollut Bull 33(7–12):226–238

    Google Scholar 

  • SPSS for Windows (2009) Rel. 17.0.3. 2009. SPSS Inc, Chicago

  • StatSoft (2005) Statistica for windows. StatSoft Inc, Tulsa, OK

    Google Scholar 

  • Steele S, Mulcahy M (1999) Gametogenesis of the oyster Crassostrea gigas in southern Ireland. J Mar Biol Assess UK 79:673–686

    Article  Google Scholar 

  • Ternes T, Stumpf M, Mueller J, Haberer K, Wilken RD, Servos M (1999) Behaviour and occurrence of estrogens in municipal sewage treatment plants-1. Investigations in Germany, Canada and Brazil. Sci Tot Environ 225(1–2):81–90

    Article  CAS  Google Scholar 

  • Wu R, Sui W, Shin P (2005) Induction, adaptation and recovery of biological responses: implications for environmental monitoring. Mar Pollut Bull 51(8–12):623–634

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge funding sources including the Australian Research Council, Hunter Water, Port Stephens Council and New South Wales Industry & Investment. Also, thanks are extended to New South Wales Industry & Investment (Oyster Hatchery, Taylors Beach) for their assistance in establishing and maintaining the laboratory trial, in particular Ben Finn, Michael Dove, Kyle Johnston, Steve O’Connor and Lynne Foulkes for maintaining the aquaria, algae stock and assisting with sample preparations. Thank you to Tony Rothkirch from the University of Newcastle for his assistance with HPLC operation.

Author information

Authors and Affiliations

  1. School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, 2308, Australia

    M. N. Andrew, R. H. Dunstan & G. R. MacFarlane

  2. New South Wales Industry & Investment, Port Stephens Research Institute, Taylors Beach, NSW, 2316, Australia

    W. A. O’Connor

Authors
  1. M. N. Andrew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. A. O’Connor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. H. Dunstan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. R. MacFarlane
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. N. Andrew.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andrew, M.N., O’Connor, W.A., Dunstan, R.H. et al. Exposure to 17α-ethynylestradiol causes dose and temporally dependent changes in intersex, females and vitellogenin production in the Sydney rock oyster. Ecotoxicology 19, 1440–1451 (2010). https://doi.org/10.1007/s10646-010-0529-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-010-0529-5

Keywords

Search

Navigation